Intensive training in adults refines A1 representations degraded in an early postnatal critical period

Zhou, Xiaoming; Merzenich, Michael M.

doi:10.1073/pnas.0707348104

Cited by 66 publications

(61 citation statements)

References 51 publications

(79 reference statements)

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“…Consistent with earlier studies (11,12), we showed that early PN exposure significantly increased the tonotopic index (degraded tonotopicity) of A1 and broadened frequency tuning (i.e., BW20) of A1 neurons. We further showed that the normalized response rates for PN-exposed rats were lower at high stimulus repetition rates (i.e., Ͼ7 pps) than in naïve rats, indicating decreased cortical responses to high-rate stimuli after noise exposure.…”

Section: Discussionsupporting

confidence: 80%

“…By contrast, previous studies that applied continuous noise exposure during the critical period reported that noise-rearing did not necessarily permanently impair cortical temporal processing into adulthood; the cortex returned to ''normal'' after animals were returned to a normal acoustic environment (13,14). A similar difference in the duration of exposure-induced plasticity has been reported in spectral domain development of A1 when rats were exposed to pulsed (11,12) or continuous (13) noise during the critical-period epoch. It has been proposed that PN-rearing prematurely advances the timing of critical-period closure for cortical plasticity, whereas continuous noise rearing, in contrast, results in the delay of criticalperiod closure.…”

Section: Discussionmentioning

confidence: 43%

“…Those changes were reversed after exposed rats were returned to normal environments (13,14). The effects on cortical spectral processing induced by exposing rats to sounds with different spectrotemporal structures have varied substantially as a function of the temporal features of the applied stimuli (10)(11)(12)(13). It remains to be determined whether or not cortical temporal information processing is influenced by early pulsed noise (PN) exposure.…”

mentioning

confidence: 99%

“…Exposing rat pups to pulsed tones of a specific frequency, for example, results in an over-representation of that frequency and broader-than-normal receptive fields in cortical field A1 (10). If rat pups are exposed to temporally modulated noises, the tonotopic organization of A1 is degraded, and there is a premature closure of the critical period (11,12). If rat pups are exposed to continuous noise, however, tonotopicity in A1 is poorly developed, and this degraded condition persists (13).…”

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confidence: 99%

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Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex

Zhou

Merzenich

2008

Proc. Natl. Acad. Sci. U.S.A.

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Studies have shown that acoustic experiences significantly contribute to the functional shaping of the structural organization and signal processing capacities of the mammalian auditory system during postnatal development. Here, we show how an early epoch of exposure to structured noise influences temporal processing in the rat primary auditory cortex documented immediately after exposure and again in adulthood. Pups were continuously exposed to broadband-pulsed noise across the critical period for auditory system development. Immediately after cessation of exposure at postnatal day Ϸ35 (P35) or Ϸ55 days later (i.e., P90) in other rats, the temporal modulation-transfer functions of cortical neurons were documented. We found that pulsed noise exposure at a low modulation rate significantly decreased cortical responses to repetitive stimuli presented across a range of higher modulation rates. The highest temporal rate at which temporal modulationtransfer function was at half of its maximum was reduced when compared with naïve rats. Low-rate pulsed noise exposure also decreased cortical response synchronization at higher stimulus rates, as shown by vector strength and Rayleigh statistic measures. These postexposure changes endured into adulthood. These findings bear significant implications for the role of early sound experiences as contributors to the ontogeny of human auditory and language-related abilities and impairments.cortical plasticity ͉ critical period ͉ temporal modulation-transfer function ͉ temporal processing S ounds in natural environments, such as animal vocalizations and human speech, have complex temporal structures. The importance of temporal structure in acoustic communication and orientation has been demonstrated in many behavioral, psychological, and neurophysiological studies. The auditory cortex plays a critical role in the perception of time-varying features of aural speech and of other complex acoustic stimuli. In humans, speech comprehension is correlated with responses of cortical neurons to temporal envelopes of speech (1), and individuals with impaired language abilities have impaired successive signal evoked cortical responses (2, 3).Earlier studies in different subprimate animal species have shown that cortical neurons display different temporal filtering properties (e.g., low-pass, responding to sound trains below certain rates, or band-pass, responding best to a specific rate, etc.) (4-7). In general, cortical neurons respond to repetitive sounds at far lower rates and with poorer temporal precision when compared with auditory nerve fibers or neurons in subcortical auditory nuclei and, in most mammalian species, are not able to follow individual sound presented at rates faster than Ϸ20 pulses per second (pps). It has been argued that for those more rapidly occurring stimuli (e.g., stimuli with repetition rate Ͼ100 pps), cortical neurons might apply a rate code instead of a temporal code (stimulus-synchronized responses) to represent the temporal structure (7). Most natural sounds, ...

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Section: Discussionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 43%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex

Zhou

Merzenich

2008

Proc. Natl. Acad. Sci. U.S.A.

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“…Consistent with earlier studies (6,7), the frequency representation of A1 determined using a conventional mapping procedure was complete and orderly in control rats, with isofrequency representational bands oriented approximately orthogonal to an orderly sound frequency representational (tonotopic) gradient ( Fig. 2 Top Left).…”

Section: Resultssupporting

confidence: 71%

Successive-signal biasing for a learned sound sequence

Zhou

Villers-Sidani

Panizzutti

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Adult rats were trained to detect the occurrence of a two-element sound sequence in a background of nine other nontarget sound pairs. Training resulted in a modest, enduring, static expansion of the cortical areas of representation of both target stimulus sounds. More importantly, once the initial stimulus A in the target A-B sequence was presented, the cortical "map" changed dynamically, specifically to exaggerate further the representation of the "anticipated" stimulus B. If B occurred, it was represented over a larger cortical area by more strongly excited, more coordinated, and more selectively responding neurons. This biasing peaked at the expected time of B onset with respect to A onset. No dynamic biasing of responses was recorded for any sound presented in a nontarget pair. Responses to nontarget frequencies flanking the representation of B were reduced in area and in response strength only after the presentation of A at the expected time of B onset. This study shows that cortical areas are not representationally static but, to the contrary, can be biased moment by moment in time as a function of behavioral context. cortical representation | perceptual training | plasticity | primary auditory cortex S uccessive-signal biasing ("prediction"), which is manifested in many behavioral studies in psychoacoustics and linguistics, very significantly contributes to the reception and production of rapidly successive inputs or actions (1-5). This study was designed to begin to reveal fundamental auditory system processes that could account for that biasing. Our primary initial goal was to apply a strategy in training by which an adult rat would be listening for the occurrence of specific stimuli in the context of (cued by the presentation of) other specific stimuli. In this initial study, we trained adult rats to respond to mark their recognition of the occurrence of a specific two-sound sequence, with the onsets of those sounds separated by 300 ms. We reasoned that in the context of this training, the rat might be biased for ("listen for" or "expect") the first sound stimulus, A. If and only if it occurred, cortical networks would hypothetically be biased to favor the reception of the second component of the target-pair stimulus, B.These studies show that training resulted in a modest static expansion of the representation of both sound elements of the target pair and, if and only if the first sound element of the target sound pair was delivered, in significant response biasing selective for the second sound stimulus in the target sequence. ResultsBehavioral Training. Rats in an experimental group (n = 6) were trained to identify a two-element auditory stimulus target presented with nine nontarget pairs (Fig. 1A) to receive food rewards. All initial stimuli in each pair were tones 200 ms in duration presented at 1.5, 3, 7, or 10 kHz. The initial stimulus in a target stimulus pair was 3 kHz (referred to as A). The second stimulus in each pair could again be 1.5, 3, 7, or 10 kHz. Second stimuli were 50 ms in duratio...

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Unintended Consequences of White Noise Therapy for Tinnitus—Otolaryngology's Cobra Effect

Attarha

Bigelow

Merzenich

2018

JAMA Otolaryngol Head Neck Surg

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Intensive training in adults refines A1 representations degraded in an early postnatal critical period

Cited by 66 publications

References 51 publications

Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex

Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex

Successive-signal biasing for a learned sound sequence

Unintended Consequences of White Noise Therapy for Tinnitus—Otolaryngology's Cobra Effect

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